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Parathyroid hormone-related protein production in the lamprey Geotria australis: developmental and evolutionary perspectives

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Abstract

This study explored the distribution of parathyroid hormone-related protein (PTHrP) and its mRNA in tissues of the lamprey Geotria australis, a representative of one of the two surviving groups of an early and jawless stage in vertebrate evolution. For this purpose, antibodies to N-terminal and mid-molecule human PTHrP were used to determine the locations of the antigen. Sites of mRNA production were demonstrated by in situ hybridisation with a digoxigenin-labelled riboprobe to exon VI of the human PTHrP gene. The results revealed that antigen and its mRNA were widely distributed among similar sites of tissue localisation to those described for mammalian and avian species. However, some novel sites of localisation, such as in the gill and notochord, were also found. Some differences in PTHrP localisation were noted among individuals at different intervals of the life cycle, indicating that the distributions of PTHrP, and possibly its roles, change with the stage of development in this species. The widespread tissue distribution in G. australis implies diverse physiological roles for this protein. The presence of PTHrP in the lamprey, a representative of a group of vertebrates, which apparently evolved over 540 million years ago, strongly suggests that it is a protein of ancient origin. In addition, the successful use of antibodies and probes based on the human sequence in the lamprey also provides evidence that the PTHrP molecule may have been conserved from lampreys through to humans.

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References

  • Bartels H, Schewe H, Potter IC (1993) Structural changes in the apical membrane of lamprey chloride cells after acclimation to seawater. Am J Physiol 265:C733–C739

    PubMed  CAS  Google Scholar 

  • Burton DW, Brandt DW, Deftos LJ (1994) Parathyroid hormone-related protein in the cardiovascular system. Endocrinology 135:253–261

    Article  PubMed  CAS  Google Scholar 

  • Chailleux N, Milet C, Vidal A, Lopez E (1995) Presence of PTH-like and PTH-related peptide-like molecules in submammalian vertebrates. Neth J Zool 45:248–250

    Google Scholar 

  • Danks JA, Ebeling PR, Hayman J, Chou ST, Moseley JM, Dunlop J, Kemp BE, Martin TJ (1989) Parathyroid hormone-related protein: immunohistochemical localisation in cancers and in normal skin. J Bone Miner Res 4:273–278

    PubMed  CAS  Google Scholar 

  • Danks JA, Devlin AJ, Ho PMW, Diefenbach-Jagger H, Power DM, Canario A, Martin TJ, Ingleton PM (1993) Parathyroid hormone-related protein is a factor in normal fish pituitary. Gen Comp Endocrinol 92:201–212

    Article  PubMed  CAS  Google Scholar 

  • Danks JA, McHale JC, Martin TJ, Ingleton PM (1997) Parathyroid hormone-related protein in tissues of the emerging frog (Rana temporaria): immunohistochemistry and in situ hybridisation. J Anat 190:229–238

    Article  PubMed  CAS  Google Scholar 

  • Danks JA, Hubbard PC, Balment RC, Ingleton PM, Martin TJ (1998) Parathyroid hormone-related protein localisation in tissues of freshwater and saltwater-acclimatized flounder. Ann NY Acad Sci 839:503–505

    Article  CAS  Google Scholar 

  • Danks JA, Ho PMW, Notini AJ, Katsis F, Hoffmann P, Kemp BE, Martin TJ, Zajac JD (2003) Identification of a parathyroid hormone in the fish, Fugu rubripes. J Bone Miner Res 18:1326–1331

    Article  PubMed  CAS  Google Scholar 

  • Donald JA, Vomachka AJ, Evans DH (1992) Immunohistochemical localisation of natriuretic peptides in the brains and hearts of the spiny dogfish Squalus acanthias and the Atlantic hagfish Myxine glutinosa. Cell Tissue Res 270:535–545

    Article  PubMed  CAS  Google Scholar 

  • Echelard Y, Epstein DJ, St Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417–1430

    Article  PubMed  CAS  Google Scholar 

  • Flanagan JA, Power DM, Bendell LA, Guerreiro PM, Fuentes J, Clark MS, Canario AVM, Danks JA, Brown BL, Ingleton PM (2000) Cloning of the cDNA for sea bream (Sparus aurata) parathyroid hormone-related protein. Gen Comp Endocrinol 118:373–382

    Article  PubMed  CAS  Google Scholar 

  • Gensure RC, Ponugoti B, Gunes Y, Papasani MR, Lanske B, Bastepe M, Rubin DA, Juppner H (2003) Identification and characterization of two PTH-like molecules in zebrafish. Endocrinology 145:1634–1639

    Article  PubMed  CAS  Google Scholar 

  • Hardisty MW (1971) Gonadogenesis, sex differentiation and gametogenesis. In: Hardisty MW, Potter IC (eds) The biology of lampreys. Academic, London, pp 295–359

    Google Scholar 

  • Hardisty MW, Potter IC, Hilliard RW (1986) Gonadogenesis and sex differentiation in the Southern Hemisphere lamprey, Geotria australis Gray. J Zool Lond (A) 209:477–499

    Google Scholar 

  • Hardisty MW, Potter IC, Hilliard RW (1989) Physiological adaptations of the living agnathans. Trans R Soc Edinb Earth Sci 80:241–254

    Google Scholar 

  • Harvey S, Wang R (1996) Parathyroid hormone and neural calcium regulation: phylogenetic perspectives. In: Dacke C, Danks J, Caple I, Flik G (eds) The comparative endocrinology of calcium regulation. Journal of Endocrinology Ltd, Bristol, pp 3–15

    Google Scholar 

  • Harvey S, Zeng YY, Pang PKT (1987) Parathyroid hormone-like immunoreactivity in fish plasma and tissues. Gen Comp Endocrinol 68:136–146

    Article  PubMed  CAS  Google Scholar 

  • Henderson JE, He B, Goltzman D, Karaplis AC (1995) Nucleolar localisation of parathyroid hormone-related protein enhances survival of chondrocytes under conditions that promote apoptotic cell death. Mol Cell Biol 15:4064–4075

    PubMed  CAS  Google Scholar 

  • Hilliard RW, Potter IC (1988) Morphology of the exocrine pancreas of the Southern Hemisphere lamprey, Geotria australis, and changes during metamorphosis. J Morphol 197:33–52

    Article  PubMed  CAS  Google Scholar 

  • Hilliard RW, Epple A, Potter IC (1985) The morphology and histology of the endocrine pancreas of the Southern Hemisphere lamprey, Geotria australis Gray. J Morphol 184:253–261

    Article  PubMed  CAS  Google Scholar 

  • Hogan BM, Danks JA, Layton JE, Hall NE, Heath JK, Lieschk GJ (2005) Duplicate zebrafish pth genes are expressed in the lateral line and central nervous system during embryogenesis. Endocrinology 146:547–551

    Article  PubMed  CAS  Google Scholar 

  • Ingham PW, McMahon AP (2001) Hedgehog signalling in animal development: paradigms and principles. Genes Dev 15:3059–3087

    Article  PubMed  CAS  Google Scholar 

  • Ingleton PM, Danks JA (1996) Distribution and functions of parathyroid hormone-related protein in vertebrate cells. Int Rev Cyt 166:231–280

    Article  CAS  Google Scholar 

  • Ingleton PM, Hazon N, Ho PMW, Martin TJ, Danks JA (1995) Immunodetection of parathyroid hormone-related protein in plasma and tissues of an elasmobranch (Scyliorhinus canicula). Gen Comp Endocrinol 98:211–218

    Article  PubMed  CAS  Google Scholar 

  • Jüppner H, Abou Samra AB, Freeman M, Kong XF, Schipani E, Richards J, Kolakowski LFJ, Hock J, Potts JT, Kronenberg HM, Segre GV (1991) A G protein-linked receptor for parathyroid hormone-related peptide. Science 254:1024–1026

    Article  PubMed  Google Scholar 

  • Kaneko T, Pang PKT (1987) Immunocytochemical detection of parathyroid hormone-like substance in the goldfish brain and pituitary. Gen Comp Endocrinol 68:147–152

    Article  PubMed  CAS  Google Scholar 

  • Kartsogiannis V, Moseley J, McKelvie B, Chou ST, Hards DK, Ng KW, Martin TJ, Zhou H (1997) Temporal expression of PTHrP during endochondral bone formation in mouse and intramembranous bone formation in an in vivo rabbit model. Bone 21:385–392

    Article  PubMed  CAS  Google Scholar 

  • Kloas W, Flugge G, Fuchs E, Stolte H (1988) Binding site for atrial natriuretic peptide in the kidney and aorta of the hagfish (Myxine glutinosa). Comp Biochem Physiol 91A:685–688

    Article  CAS  Google Scholar 

  • Lam MHC, Olsen SL, Rankin WA, Ho PMW, Martin TJ, Gillespie MT, Moseley JM (1997) PTHrP and cell division: expression and localisation of PTHrP in a keratinocyte cell line (HaCaT) during the cell cycle. J Cell Physiol 173:433–446

    Article  PubMed  CAS  Google Scholar 

  • Lethbridge RC, Potter IC (1981) The skin. In: Hardisty MW, Potter IC (eds) The biology of lampreys. Academic, London, pp 377–447

    Google Scholar 

  • Martin TJ, Moseley JM, Williams ED (1997) Parathyroid hormone-related protein: hormone and cytokine. J Endocrinol 154:S23–S37

    PubMed  CAS  Google Scholar 

  • Massfelder T, Dann P, Wu TL, Vasavada R, Helwig JJ, Stewart AF (1997) Opposing mitogenic and anti-mitogenic actions of parathyroid hormone-related protein in vascular smooth muscle cells: a critical role for nuclear targeting. Proc Natl Acad Sci U S A 94:13630–13635

    Article  PubMed  CAS  Google Scholar 

  • Moseley JM, Gillespie MT (1995) Parathyroid hormone-related protein. Crit Rev Clin Lab Sci 32:299–343

    Article  PubMed  CAS  Google Scholar 

  • Moseley JM, Kubota M, Diefenbach-Jagger H, Wettenhall REH, Kemp BE, Suva LJ, Rodda CP, Ebeling PR, Hudson PJ, Zajac JD, Martin TJ (1987) Parathyroid hormone-related protein purified from a human lung cancer cell-line. Proc Natl Acad Sci U S A 84:5048–5052

    Article  PubMed  CAS  Google Scholar 

  • Moseley JM, Hayman JA, Danks JA, Alcorn D, Grill V, Southby J, Horton, MA (1991) Immunohistochemical detection of parathyroid hormone-related protein (PTHrP) in human fetal epithelia. J Clin Endocrinol Metab 73:478–483

    Article  PubMed  CAS  Google Scholar 

  • Okabe M, Graham A (2004) The origin of the parathyroid gland. Proc Natl Acad Sci U S A 101:17716–17719

    Article  PubMed  CAS  Google Scholar 

  • Pang PKT, Kaneko T, Harvey S (1988) Immunocytochemical distribution of PTH immunoreactivity in vertebrate brains. Am J Physiol 255:R643–R647

    PubMed  CAS  Google Scholar 

  • Peek WD, Youson JH (1979) Ultrastructure of chloride cells in young adults of the anadromous sea lamprey, Petromyzon marinus L., in freshwater and during adaptation to seawater. J Morphol 160:143–164

    Article  PubMed  CAS  Google Scholar 

  • Philbrick WM, Wysolmerski JJ, Galbraith S, Holt E, Orloff JJ, Yang KH, Vasavada RC, Weir EC, Broadus AE, Stewart AF (1996) Defining the roles of parathyroid hormone-related protein in normal physiology. Physiol Rev 76:127–173

    PubMed  CAS  Google Scholar 

  • Potter IC, Hilliard RW (1986) Growth and the average duration of larval life in the Southern Hemisphere lamprey, Geotria australis. Experientia 42:1170–1173

    Article  Google Scholar 

  • Potter IC, Hilliard RW, Bird DJ (1980) Metamorphosis in the Southern Hemisphere lamprey, Geotria australis. J Zool Lond 190:405–430

    Article  Google Scholar 

  • Potter IC, Hilliard RW, Bird DJ, Macey DJ (1983) Quantitative data on morphology and organ weights during the protracted spawning-run period of the Southern Hemisphere lamprey, Geotria australis. J Zool Lond 200:1–20

    Article  Google Scholar 

  • Shu D-G, Luo H-L, Conway Morris S, Zhang X-L, Chen L, Han J, Zhu M, Li Y, Chen L-Z (1999) Lower cambrian vertebrates from southern China. Nature 402:42–46

    Article  CAS  Google Scholar 

  • St Jacques B, Hammerschmidt M, McMahon AP (1999) Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13:2072–2086

    PubMed  CAS  Google Scholar 

  • Suva LJ, Winslow GA, Wettenhall REH, Hammonds RG, Moseley JM, Diefenbach-Jagger H, Rodda CP, Kemp BE, Rodriguez H, Chen EY, Hudson PJ, Martin TJ, Wood WI (1987) A parathyroid hormone-related protein implicated in malignant hypercalcemia: cloning and expression. Science 237:893–896

    Article  PubMed  CAS  Google Scholar 

  • Toop T, Donald JA, Evans DH (1995) Natriuretic peptide receptors in the kidney and the ventral and dorsal aortae of the Atlantic hagfish Myxine glutinosa (Agnatha). J Exp Biol 198:1875–1882

    PubMed  CAS  Google Scholar 

  • Trivett MK, Officer RA, Clement JG, Walker TI, Joss JM, Ingleton PM, Martin TJ, Danks JA (1999) Parathyroid hormone-related protein (PTHrP) in cartilaginous and bony fish tissues. J Exp Zool 284:541–548

    Article  PubMed  CAS  Google Scholar 

  • Trivett MK, Walker TI, Macmillan DL, Clement JG, Martin TJ, Danks JA (2002) Parathyroid hormone-related protein (PTHrP) production sites in elasmobranches. J Anat 201:41–52

    Article  PubMed  CAS  Google Scholar 

  • Vasavada RC, Cavaliere C, D'Ercole AJ, Dann P, Burtis WJ, Madlener AL, Zawalich K, Zawalich W, Philbrick W, Stewart AF (1996) Overexpression of parathyroid hormone-related protein in the pancreatic islets of transgenic mice causes islet hyperplasia, hyperinsulinemia, and hypoglycemia. J Biol Chem 271:1200–1208

    Article  PubMed  CAS  Google Scholar 

  • Vortkamp A, Lee K, Lanske B, Segre GV, Kronenberg HM, Tabin C (1996) Indian hedgehog and parathyroid hormone-related protein regulate the rate of cartilage differentiation. Science 273:613–622

    Article  PubMed  CAS  Google Scholar 

  • Wysolmerski JJ, Stewart AF (1998) The physiology of parathyroid hormone-related protein: an emerging role as a developmental factor. Annu Rev Physiol 60:431–460

    Article  PubMed  CAS  Google Scholar 

  • Youson JH (1981) The kidneys. In: Hardisty MW, Potter IC (eds) The biology of lampreys. Academic, London, pp 191–261

    Google Scholar 

  • Zhou H, Choong PFM, McCarthy R, Chou ST, Martin TJ, Ng KW (1994) In situ hybridisation to show sequential expression of osteoblast gene markers during bone formation in vivo. J Bone Miner Res 9:1489–1499

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

JAD is a Senior Research Fellow of the National Health and Medical Research Council, Australia. We would like to thank John Youson for his valuable assistance, David Paul (Department of Zoology) for his help with photomicrography and preparation of the figures and Daphne Hards (St. Vincent's Institute of Medical Research) for the help with histology.

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Correspondence to Janine A. Danks.

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Communicated by M. Hammerschmidt

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Trivett, M.K., Potter, I.C., Power, G. et al. Parathyroid hormone-related protein production in the lamprey Geotria australis: developmental and evolutionary perspectives. Dev Genes Evol 215, 553–563 (2005). https://doi.org/10.1007/s00427-005-0015-x

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